Memory, Subjective Memory and Motor Functioning in Non-Demented Elders With and Without Parkinson’s Disease

Parkinson’s Disease (PD) is a progressive degenerative condition defined by characteristic motor symptoms (e.g., bradykinesia, tremor, rigidity). However, non-motor symptoms, such as cognitive deficits (e.g., dementia, memory deficits, reduced impulse control) and behavioral disorders (e.g., depression, anxiety, apathy) are common even in the early stages of PD (Postuma et al., 2015; Rieu et al., 2016). Cognitive impairments typically involve visuo-spatial perception, working memory (e.g., active sequential information processing), executive functions (e.g., inhibition, planning, attentional set shifting) and declarative (e.g., episodic) memory (Di Rosa et al., 2017; Dubois & Pillon, 1996; see also Papagno & Trojano, 2018). During disease progression, cognitive (e.g., memory loss, word-retrieval difficulties) and behavioral (e.g., depression) symptoms become more tightly coupled as worsening balance and gait deficits increasingly restrict patients’ independence and quality of life (Barbosa et al., 2016; Bohnen & Cham, 2006; Dirnberger & Jahanshahi, 2013). Indeed, cognitive resources are necessary to process and integrate sensory and motor information and to plan the motor responses for maintaining balance (e.g., Kelly et al., 2015). There is evidence that working memory performance of individuals with PD is negatively impacted by the occurrence of depressive signs (Foster, Yung, Drago, Crucian, & Heilman, 2013) and that cognitive performance, primarily working memory and/or executive functioning, has been found to predict various behavioral outcomes in PD patients including risk of falling (Barbosa et al., 2016). Overall, the pervasive impact of PD symptoms is widely recognized to significantly impair life quality, especially in the advanced stages of the disease (e.g., Chrischilles, Rubenstein, Voelker, Wallace, & Rodnitzky, 1998; The Global Parkinson’s Disease Survey [GPDS] Steering Committee, 2001; Rieu et al., 2016).

While mnemonic processes such as working memory and declarative memory are crucial for many the day-to-day activities (e.g., naming objects, learning new words, remembering an appointment) measures of subjective memory are increasingly appreciated as important sources of information about informants’ risk of actual cognitive decline and awareness of cognitive functioning. Despite such recognition there have been relatively few studies of subjective memory and working memory in PD and no clear pattern of findings has emerged. This is significant since various aspects of subjective and objective memory are likely to play an important role in patient life quality, such as remembering to take medication, a crucial element in the daily life of a person with a chronic disease (Gould, McDonald-Miszezak, & King, 1997; Park & Mayhorn, 1996). A further reason why the investigation of subjective memory and mnestic efficiency in individual with PD is relevant is that memory complaints may reflect emerging functional brain abnormalities not easily detected via objective memory tasks. Furthermore, objective memory measures may identify individuals lacking awareness of mnestic impairment.

However, the existing literature is quite mixed even with respect to which aspects of subjective memory are impaired in PD (Ivory, Knight, Longmore, & Caradoc-Davies, 1999; Sitek et al., 2011; Souchay, Isingrini, & Gil, 2006). For instance, Sitek et al. (2011) observed accurate self-assessment of memory performance in PD both in relation to objective memory performance and the judgements of proxies. In contrast, Souchay et al. (2006) reported that while both healthy controls and people with PD underestimated their capacity to recall a set of words (i.e., global predictions of memory, when participants were asked to judge the likelihood of recall separately for each item, the group with PD overestimated memory accuracy. In addition, there are reports indicating that individuals with PD make less use of external (i.e., based on the use of environmental cues) memory strategies (e.g., diary, shopping list) than matched healthy controls, perhaps because such aids require greater fine motor efficiency (e.g., writing) (Johnson, Pollard, Vernon, Tomes, & Jog, 2005). Finally, the impact of PD on everyday cognitive performance may be selective rather than global. Poliakoff and Spark (2008) reported what while there was a non-significant increase in overall cognitive failures, significant increases on specific items related to distractibility and clumsiness were evident.

While increased clarity concerning the impact of PD on objective and subjective memory and the relationship between them is highly desirable, such a goal is complicated by confounding variance in depressive symptomatology (Dumas & Newhouse, 2015; Fastame, 2014). This is rarely considered in PD samples and, when it has, findings have been mixed (Coutler, 1989; Reynolds, Hanna, Neargarder, & Cronin-Golomb, 2017; Sitek et al., 2011). For instance, Sitek et al. (2011) reported an overestimation of memory defects in PD group due to self-reported depressive symptoms. In contrast, Coutler (1989) found no differences in metamemory monitoring between depressed and non-depressed patients with PD when compared with non-depressed healthy controls. Findings regarding the impact of depression on working memory are similarly mixed. Some studies have found depression to negatively impact performance (Dumas & Newhouse, 2015) while other studies have found no impairment (Reynolds et al., 2017). Overall, systematic studies investigating this topic are lacking and as suggested by Pannu and Kaszniak (2005), the administration of different neuropsychological tools to patients at different disease stages is also likely to contribute to the variability in findings.

The present study was undertaken with the aim of comparing subjective and objective memory function in non-demented people with and without PD independent from variance in depressive symptoms. The relationship of working memory to motor (gait and posture) performance was also examined. In short, the main aims of the current study were to examine:

In relation to these aims the following hypotheses were tested:

We believe this is the first study that has attempted to explore the nature of the relationship among measures of memory, MFQ subscales, depression and motor functioning in a sample of elders with and PD at the early stages. Such investigation in the early stages of the disorder may yield important knowledge about intervention strategies that may improve or preserve life quality.

Method

Results

First, three separate Analyses of Covariance (ANCOVAs) were conducted to investigate the effect of group (i.e., participants with PD vs. healthy controls) on Forward Digit Span test, Backward Digit Span Test and vocabulary test conditions, in each case, controlling for the effect of self-reported depression. The effect of CES-D was not significant in any of the memory conditions, F(1,51) = 1.58, p = .21 for Forward Digit Span, F(1,51) = 2.78, p = .10 for Backward Digit Span and F(1,51) = 2.94, p = .09, respectively. The main effect of group was significant in terms of Forward, F(1,51) = 4.28, p = .04, ${\mathrm{\eta }}_{\mathrm{p}}^2$ = .08, and Backward, F(1,51) = 4.61, p = .04, ${\mathrm{\eta }}_{\mathrm{p}}^2$ = .08, Digit Span and Vocabulary, F(1,51) = 4.41, p = .04, ${\mathrm{\eta }}_{\mathrm{p}}^2$ = .08, efficiency. Controls outperformed participants with PD in Forward Digit Span (M = 6.72, SD = 1.5 vs. M = 5.69, SD = 1.9), Backward Digit Span (M = 6.03, SD = 1.4 vs. M = 5.04, SD = 1.8) and lexical competence (M = 53.30, SD = 15.2 vs. M = 43.82, SD = 17.1).

Next, to investigate the impact of PD on the two MFQ indexes while controlling for the effect of depression and semantic memory, a Multivariate Analysis of Covariance (MANCOVA) was carried out, using group (i.e., participants with PD vs. healthy controls) as between-subject variable and CES-D and vocabulary as covariates. The multivariate tests documented the significant main effects of CES-D (Wilks’ λ = .86, df = 2; 48, p = .03) and vocabulary (Wilks’ λ = .76, df = 2; 48, p = .009), whereas the main effect of group was not significant (Wilks’ λ = .96, df = 2; 48, p = .39). No group differences were found on Seriousness of Forgetting, F(1,49) = .67, p = .42) and Mnemonic Usage, F(1,49) = .91, p = .34, sub-scales. Participants with PD had similar levels of complaints about the seriousness of their memory failures (M = 76.43, SD = 3.7, than matched controls (M = 71.90, SD = 3.8). Moreover, the clinical group reported a similar use of external and internal memory strategies (M = 29.6, SD = 2.1) compared to the healthy controls (M = 32.6, SD = 2.2). The main effect of CES-D was significant in Seriousness of Forgetting condition, F(1,50) = 7.66, p = .008, ${\mathrm{\eta }}_{\mathrm{p}}^2$ = .13, but not in Mnemonic Usage one, F(1,50) = .20, p = .66, sub-scale. A similar pattern of results was found for vocabulary, F(1,50) = 14.69, p < .0005, ${\mathrm{\eta }}_{\mathrm{p}}^2$ = .23 for Seriousness of Forgetting and F(1,50) = .0001, p = .99 for Mnemonic Usage.

Furthermore, three separate ANCOVAs where conducted to explore the impact of group on self-assessed actual memory efficiency relative to 1, 5 and 10 years before, using both CES-D and vocabulary as covariates. For self-assessed memory, relative to 1 year earlier, there were main effects of group, F(1,50) = 8.73, p = .005, ${\mathrm{\eta }}_{\mathrm{p}}^2$ = .15, and CES-D, F(1,50) = 11.83, p = .001, ${\mathrm{\eta }}_{\mathrm{p}}^2$ = .19, whereas the effect of vocabulary was not significant, F(1,50) = .47, p = .49. The same pattern was found for self-assessed memory relative to 5 years earlier, F(1,50) = 12.69, p = .001, ${\mathrm{\eta }}_{\mathrm{p}}^2$ = .20 for group; F(1,50) = 10.63, p = .002, ${\mathrm{\eta }}_{\mathrm{p}}^2$ = .17 for CES-D and F(1,50) = 2.72, p = .11 for vocabulary) and to 10 years earlier, F(1,50) = 5.40, p = .02, ${\mathrm{\eta }}_{\mathrm{p}}^2$ = .10 for group; F(1,50) = 4.70, p = .03, ${\mathrm{\eta }}_{\mathrm{p}}^2$ = .09 for CES-D and F(1,50) = .03, p = .86 for vocabulary. Overall, participants with PD reported less trust in their memory functioning compared to the past. Moreover, people with PD reported more depressive signs (M = 16.44, SD = 9.31) than controls (M = 11.37, SD = 8.5). Table 2 summarizes the findings relative to all the above mentioned ANCOVAs and MANCOVA.

Then, two separate stepwise regression analyses were conducted to explore whether group (i.e., people with PD vs. controls), general cognitive efficiency (i.e., MMSE), depression (i.e., CES-D), years of education, hours per day spent for reading (i.e., ≤1 hour vs. ≥2 hours) predicted Seriousness of Forgetting and Mnemonic Usage MFQ indexes. When Seriousness of Forgetting was entered as the dependent variable, it was found that years of education (b = -0.43, t = -3.53, p = .001) and MMSE score (b = 0.29, t = 2.35, p = .02) predicted 22% of the variance in the abovementioned MFQ subscale, corrected R² = 0.22, F(1,50) = 8.38, p = .006. In contrast, none of the independent variables predicted the Mnemonic Usage measure.

To compare the impact of disease status on gait and functional mobility measures a series of t-test comparisons were conducted. The effect of group (control vs. PD) was significant for the step length, t(46) = -2.27, p = .03, and approached the significance for the time of the first 180° (intermediate) rotation in TUG, t(46) = 1.81, p = .08. The mean step length of participants with PD was shorter (M = .57, SD = 0.10) than that of matched controls (M = .67, SD = 0.21).

Finally, a series of Pearson’s product moment coefficients were computed to investigate the relationship between Forward and Backward Digit spans and the postural motor indexes. Statistically significant correlations were found between Forward Digit span and step length (r = .37, p = .009), TUG sit-to-stand time (r = -.30, p = .049), TUG stand-to-sit time (r = -.39, p = .010) and time of final 180° turning in TUG (r = -.37, p = .015), respectively. In contrast, Backward Digit span significantly correlated only with step length (r = .30, p = .037) and approached significance with overall TUG time (r = -.29, p = .057). Table 3 illustrates these outcomes.

Discussion

Only a few studies have examined the subjective memory deficits that can accompany objective memory impairment in the early stages of PD and these have yielded inconsistent findings. The present study aimed to resolve this issue via concomitant measurement of depressive symptomatology and re-examine the association between objective memory and motor function. The sample was comprised of community dwelling individuals, with or without PD, all of whom were screened for signs of global cognitive impairment. The control and PD groups were age-, education- and sex-matched yet compared to the control group displayed objective memory impairment across all indices examined; forward and backward digit spans were lower, as was performance on the vocabulary subtest of the WAIS. These tests assess distinct components of memory (passive and active working memory and semantic memory, respectively) commonly reported to be impaired in PD (Di Rosa et al., 2017; Gabrieli, Singh, Stebbins, & Goetz, 1996; Henry & Crawford, 2004). The deficit in both forward and backward digit span was somewhat unexpected since demand characteristics can influence task sensitivity (Poliakoff & Spark, 2008). Indeed, the lowest accuracy of mnestic functions of people with PD was detected when an active manipulation of verbal serial information involving executive functions was requested (i.e., Backward Digit Span Test condition), and even when a reduced amount of cognitive resources was used to retrieve the sequential strings in forward order. Similarly, despite similar education and global cognitive efficiency levels characterizing participants with and without PD, unexpectedly, differences in terms of vocabulary were found between the two groups (e.g., Matison et al., 1982; Wermuth et al., 1996). For what concerns the vocabulary performance, a possible explanation is that our participants with PD were older that those recruited by Wermuth et al. (1996) and, in turn, the aging factor could be related to the lowest efficiency of the attentional/control processes of the participants with PD that was reflected in poorer working memory functions. However, at present we cannot exclude that the lowest vocabulary efficiency of the group with PD could be the expression of a more general impairment of semantic memory (Henry & Crawford, 2004; see also Gabrieli et al., 1996) or of a specific word-finding difficulty (e.g., Matison et al., 1982) that have been observed in that clinical population. Future research has to clarify this issue by the administration of specific tasks assessing this (e.g., semantic fluency tasks).

Use of the MFQ permitted assessment of several aspects of subjective memory and revealed contrasting consequences of PD. Control and PD groups rated the seriousness of forgetting similarly and, unlike some previous research (Johnson et al., 2005), use of memory aids did not differ. These are odd outcomes given the evident impairment of objective memory and wider evidence showing that non-demented PD patients often experience difficulties completing everyday tasks (Poliakoff & Spark, 2008). Two possible interpretations can be suggested. First, the PD patients may have been unaware of their declarative and working memory deficits and, as a result, did not compensate with increased use of memory aids. However, this seems unlikely, since self-rated memory performance (relative to 1, 5 or 10 years previous) was worse in the PD group suggesting intact awareness of cognitive decline. A second, and more likely, scenario is that motivation to use memory aids was reduced. Apathy is a recognised feature of PD, known to be associated with cognitive functioning and independent from disease progression (Pluck & Brown, 2002). This would appear to provide a better explanation for the observed pattern of differences in subjective memory. Despite from these suggestions, from an applied viewpoint, the current outcomes could have serious consequences in terms of medication adherence (Gould et al., 1997) and suggest that our participants with PD could benefit of memory and metamemory interventions promoting life quality and enhancing the ability to deal with everyday problems.

One implication of these findings is that concomitant targeting of reduced motivation may be a more effective means of developing self-regulation of memory impairments in PD. Such an approach could be especially useful in those with depression (Goedeken, Potempa, Prager, & Foster, 2018) given that our findings confirmed that increased depressive symptomatology was associated with impairments of both objective and subjective memory (e.g., Dumas & Newhouse, 2015; Fastame, 2014). However, additional research in this area is needed since prior research indicates that apathy and depression are not correlated in PD (Pluck & Brown, 2002).

Moreover, education and general cognitive efficiency predict seriousness of forgetting, but not memory usage and self-reported depressive signs did not predict any MFQ measure. Overall, these outcomes are partially consistent with previous evidence (Gilewski et al., 1990; Reisberg et al., 2008) suggesting a need for further investigation.

Motor function was impaired in participants with PD, as expected; they walked with shorter steps and performed the 180° turn during the TUG task less effectively. Most previous studies on gait and mobility have reported similar gait and TUG anomalies in individuals with PD (Boonstra, van der Kooij, Munneke, & Bloem, 2008; Morris, Morris, & Iansek, 2001). That only a restricted set of motor impairments was evident is consistent with the mild disability level of the PD group (as indicated by their H&Y scale scores) and the fact that they were tested while on medication. The observed significant correlations between digit span performance and indices of gait and posture are of greater interest. Although previous studies have made similar observations (e.g., Kelly et al., 2015), the present study confirmed that these associations are independent of variance in depressive symptoms. Previous research shows that depression is frequently present in PD and that it may confound both motor and cognitive task performance (Cummings, 1992).

The most obvious limitations of the present research concern our sample and its size and composition. Participants were non-demented, community-dwelling adults with or without early-stage PD; those with PD were medicated. Overall, the sample had a relatively high education level and was actively engaged in leisure activities. Extending the findings beyond this small homogenous group requires further, larger scale investigation. A further point is that the sample was recruited in Sardinia, a region in which the prevalence of PD is reduced compared to the mainland Italy and Northern Europe (Pupillo et al., 2016; Rosati et al., 1980). Perhaps of greater significance is that older adults from this region have consistently been found to display unusual psychological characteristics relative to age-matched peers. These include some attributes examined in the present study (e.g., Fastame, Hitchcott, & Penna, 2015; Fastame & Penna, 2014; Hitchcott et al., 2017; Hitchcott, Fastame, & Penna, 2018) and the extent to which this influenced the present findings is unclear without further investigation. In conclusion, future research extending these findings to broader groups with PD and investigation of the neural substrates underpinning the metamemory dimensions explored in the current study would be useful.